Jorge B. Torres

Canopy- and Ground-Dwelling Predatory Arthropods in Commercial Bt and non-Bt Cotton Fields: Patterns and Mechanisms

Abstract Abundance of canopy- and ground-dwelling predators was monitored in three pairs of commercial Bt and non-Bt cotton fields (5–15 ha) during three successive seasons using three sampling methods: bagged whole plants, drop cloth samples, and pitfall traps. Samples were taken throughout each growing season. Insecticides were applied to manage pests when economic thresholds were exceeded in both cotton types. Of 1,518 possible date-by-date orthogonal contrasts used to evaluate abundance of predators in all sampling methods, analysis of variance generated 23 contrasts with greater abundance in non-Bt and 20 with greater abundance in Bt cotton, comprising nine taxa. When data from all three seasons were pooled for each sampling method, only six contrasts comprising five taxa were significant, with two favoring Bt (Nabis spp. in whole plant inspections and spiders in drop cloths) and four favoring non-Bt cotton [Hippodamia convergens Guérin-Méneville in drop cloths and whole plant inspections and lady beetle eggs and Geocoris uliginosus (Say) in whole plant inspections]. The shift in abundance of canopy-dwelling taxa—especially coccinellids—between Bt and non-Bt cotton fields was likely associated with insecticide use. Analyses of predator community dynamics using principal response curves showed that the abundance of ground-dwelling predators was not affected by cotton type, whereas abundance of canopy predators varied across seasons with no particular trend for either cotton type. The abundance of predators across 3 yr in cotton fields with standard grower practices failed to exhibit any negative impact of Bt cotton on predator populations.

Interactions of Bacillus thuringiensis Cry1Ac toxin in genetically engineered cotton with predatory heteropterans

A number of cotton varieties have been genetically transformed with genes from Bacillus thuringiensis (Bt) to continuously produce Bt endotoxins, offering whole plant and season-long protection against many lepidopteran larvae. Constant whole-plant toxin expression creates a significant opportunity for non-target herbivores to acquire and bio-accumulate the toxin for higher trophic levels. In the present study we investigated movement of Cry1Ac toxin from the transgenic cotton plant through specific predator-prey pairings, using omnivorous predators with common cotton pests as prey: (1) the beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae), with the predator Podisus maculiventris (Heteroptera: Pentatomidae); (2) the two-spotted spider mite, Tetranychus urticae (Acarina: Tetranychidae), with the predatory big-eyed bug Geocoris punctipes (Heteroptera: Geocoridae) and (3) with the predatory damsel bug Nabis roseipennis (Heteropera: Nabidae); and (4) the thrips Frankliniella occidentalis (Thysanoptera: Thripidae) with the predatory pirate bug Orius insidiosus (Heteroptera: Anthocoridae). We quantified Cry1Ac toxin in the cotton plants, and in the pests and predators, and the effects of continuous feeding on S. exigua larvae fed either Bt or non-Bt cotton on life history traits of P. maculiventris. All three herbivores were able to convey Cry1Ac toxin to their respective predators. Among the herbivores, T. urticae exhibited 16.8 times more toxin in their bodies than that expressed in Bt-cotton plant, followed by S. exigua (1.05 times), and F. occidentalis immatures and adults (0.63 and 0.73 times, respectively). Of the toxin in the respective herbivorous prey, 4, 40, 17 and 14% of that amount was measured in the predators G. punctipes, P. maculiventris, O. insidiosus, and N. roseipennis, respectively. The predator P. maculiventris exhibited similar life history characteristics (developmental time, survival, longevity, and fecundity) regardless of the prey’s food source. Thus, Cry1Ac toxin is conveyed through non-target herbivores to natural enemies at different levels depending on the herbivore species, but continuous lifetime contact with the toxin by the predator P. maculiventris through its prey had no effect on the predator’s life history. The results found here, supplemented with others already published, suggest that feeding on Cry1Ac contaminated non-target herbivores does not harm predatory heteropterans and, therefore, cultivation of Bt cotton may provide an opportunity for conservation of these predators in cotton ecosystems by reducing insecticide use.

Expression of Bacillus thuringiensis Cry1Ac protein in cotton plants, acquisition by pests and predators: a tritrophic analysis

1. Studies have shown that Cry proteins of the bacterium Bacillus thuringiensis expressed in transgenic plants can be acquired by nontarget herbivores and predators. A series of studies under field and controlled conditions was conducted to investigate the extent to which Cry1Ac protein from Bt transgenic cotton reaches the third trophic level and to measure the amount of protein that herbivores can acquire and expose to predators.

Toxicity of thiamethoxam and imidacloprid to Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) nymphs associated to aphid and whitefly control in cotton

The toxicity of thiamethoxam and imidacloprid to Podisus nigrispinus (Dallas) nymphs, and their efficacy against whitefly and cotton aphid were studied. Thiamethoxam and imidacloprid were 217.6 and 223.4 and 1435.2 and 346.8 times more toxic (LC90) by ingestion than by residual contact to 2nd- and 5th-instar nymphs of this predator, respectively. Nymphs caged on potted cotton plants and treated with either insecticide at 1 mg (a.i.) per plant or more had lower survival than those on untreated plants, up to day 52 after treatment. Thiamethoxam and imidacloprid reduced field survival of P. nigrispinus compared to untreated plants up to nine days after treatment. Thiamethoxam and imidacloprid showed significant control of whitefly in comparison with untreated plants up to 40 days after treatment in potted plants. Whitefly population had low density over time in the field with no differences between treatments and only at day 64 higher whitefly population was observed on untreated plants and plants treated with 0.5 mg (a.i.) of thiamethoxam per plant. Plots treated with thiamethoxam and imidacloprid at doses over 1 mg (a.i.) per plant retained aphid infestation lower than 10% up to 61 days of plant age. Untreated and treated plants with 0.5 mg of thiamethoxam showed infestation of 68.7 and 31.2%, respectively, at this time. Thiamethoxam and imidacloprid used in cotton for whitefly and aphid control aiming P. nigrispinus preservation can be more successful when they are used at doses bellow 1 mg (a.i.) per plant due to shorter residual effect.

Oviposição, desenvolvimento e reprodução de Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) em diferentes hospedeiros de importância econômica

The host selection for oviposition by Spodoptera frugiperda (J.E. Smith) among corn, millet, cotton and soybean, and its relationship with the biological characteristics were investigated. Free and non-choice tests for oviposition using plots containing five plants each, from each host in plastic greenhouse, resulted in similar oviposition preference among the host plants. In addition, selected biological characteristics of S. frugiperda were determined in the laboratory with larvae feeding on host leaves, and the combination of leaf and cotton boll. Neonate larvae exhibited low success of colonization on cotton boll compared to the leaves of all other hosts. Spodoptera frugiperda fed only on cotton bolls exhibited longer larval and pupal development, and longer adult life span; however with similar egg production. Larvae fed cotton leaves during six days and then transferred to cotton bolls, however, exhibited development and reproduction similar to those reared on corn or only on cotton leaves. Therefore, the variations on immature stages of S. frugiperda were not related with host selection for oviposition which was similar among the studied hosts. Based on our data, the millet as a winter, rotational, and cover crop is a potential host for S. frugiperda, while leaves and cotton bolls were diets of intermediate suitability as compared to corn and soybean leaves.

Nymphal development and adult reproduction of the stinkbug predator Podisus nigrispinus (Het., Pentatomidae) under fluctuating temperatures

Abstract: Developmental rates, egg and nymph survival and adult reproduction of Podisus nigrispinus (Dallas) (Het., Pentatomidae) were investigated under six fluctuating temperatures and night–day regimes with a photoperiod of 14 h light: 10 h dark compared with a check temperature of 27 ± 1.5°C. Lower development threshold temperatures for egg, nymphal stage and from egg to adult were estimated at 13.70, 11.96 and 12.68°C with a requirement, respectively, of 54.34, 284.25 and 327.13 degree‐days. The highest egg‐adult development rate was achieved at 25–35°C. At 10–20°C only 7.0% of nymphs reached adult stage, whereas at 27, 15–25 and 17–27°C, 93.0, 87.3 and 91.1% adult emergence was achieved, respectively. The females that emerged at 10–20°C laid no eggs, while those ar 25–35, 15–25, 17–27 and 27°C produced a total of 92.1, 453.2, 415.0 and 325.0 eggs, respectively. Results for threshold temperature and thermal requirement were approximately those reported at constant temperatures by other researchers, while the reproductive parameters of P. nigrispinus were better at intermediate temperatures ranging from 15–25 to 20–30°C.

Zoophytophagous pentatomids feeding on plants and implications for biological control

Zoophytophagous insects can feed on a variety of prey, plants and plant products. By studying the interactions between predatory hemipterans and plants harbouring the prey of these insects, scientists have started to establish two potential outcomes: (1) positive effects like the enhancement of their life history characteristics by acquiring plant contents; and (2) negative effects mediated by plant resistance to herbivores or prey ingesting secondary plant metabolites. Despite this research, there is a lack of information about the feeding sites of predatory hemipterans on their host plants, what they ingest from plants, and whether they cause damage to their host plants. The results presented here indicate that the xylem is one of the feeding sites of predatory hemipterans on plants. The dissection of predators that fed on plants with marked vessels and testing insects for the presence of Cry protein constitutively expressed in the cytoplasm of plant cells revealed that bugs are not able to acquire cytoplasm contents from the plant cell. In addition, we demonstrate that systemic insecticide circulating inside plants from soil applications contaminates these predators. Our results are discussed in the context of zoophytophagous feeding behaviour exhibited by predatory hemipterans and the use of systemic insecticides for the conservation of natural enemies. This interaction contradicts the concept of ecological selectivity obtained for natural enemies through the placement of systemic insecticide in the soil as a selective method of deploying chemical control and predatory hemipteran conservation within the integrated pest management framework.

Dispersal of Podisus nigrispinus (Het., Pentatomidae) nymphs preying on tomato leafminer: effect of predator release time, density and satiation level

Abstract:  The dispersal potential of nymphal stinkbug, Podisus nigrispinus (Dallas, 1851) (Het., Pentatomidae) preying on larvae of the tomato leafminer Tuta absoluta (Meyrick, 1917) (Lep., Gelechiidae) was studied in an open‐sided greenhouse. The parameters investigated were (1) the density of nymphs released per plant (one or five); (2) the release time (0600 and 1800 h); and (3) predator satiation level (satiated and 24‐h‐starved nymphs). Tomato plants were infested with larvae of the tomato leafminer (one third or fourth instar per leaf). The evaluations started 30 min after the release of predators second instar and hourly evaluations were carried out over 36 and 24 h for release times of 0600 and 1800 h, respectively. Starved nymphs released in the morning, either alone or in groups of five, dispersed faster than satiated nymphs. All of the starved individuals had left the plant by the end of the observation period, whereas 25 and 36% of the satiated nymphs released alone and in groups, respectively, stayed on the plant until the end of the observation period. Both satiated and starved nymphs showed slower rates of dispersal when released at 1800 h. Satiated nymphs delayed prey attack up to 9 h, whereas starved individuals started to attack T. absoluta caterpillars 1 h after their release at both densities. Our findings suggest more effective biological control of T. absoluta is possible with the release of second instar nymphs of P. nigrispinus when starved for 24 h prior to release and then released either in the morning or in the evening.

Development of Spodoptera frugiperda on different hosts and damage to reproductive structures in cotton.

The fall armyworm (FAW), Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), is a widespread pest species of various cultivated plants. The pest status of FAW in cotton in the Cerrado region of Brazil has increased with the recent changes in cotton crop systems, such as double cropping and the use of cover or winter crops with non‐tillage cropping systems. In this study we investigated the performance of FAW on three major crops cultivated in the Cerrado – soybean, corn, and cotton – and millet which has been integrated into the landscape as a cover crop. Further, the damage to various reproductive structures of cotton plants by FAW larvae was determined. Both studies were conducted under field conditions. Survival of FAW larvae caged on millet plants was higher than on other hosts. The FAW reared on millet also exhibited a net reproductive rate similar to that observed on corn, which was considered the best host for FAW, and the highest intrinsic rate of increase and lowest mean generation time compared to all other hosts. In cotton, the low availability of bolls during the plant’s blooming stage resulted in higher square feeding, whereas infestation during the plant’s boll stage resulted in higher loss of bolls and lower attack on squares. The number of adults produced in a generation was higher when plants were infested in the boll stage. The results indicated that FAW is a threat to cotton when bolls are available and can cause significant loss of reproductive structures. In addition, based on the FAW performance feeding on millet, this cover crop can be among the reasons of FAW increasing pest status in subsequent crops.

Biologia comparada e comportamento de Tetranychus urticae Koch (Acari: Tetranychidae) e Phytoseiulus macropilis (Banks) (Acari: Phytoseiidae) em algodoeiro bollgardTM e Isolinha não-Transgênica

The two spotted spider mite, Tetranychus urticae Koch, is a nontarget herbivore of Bt-cotton, but acquires and accumulates higher levels of Cry toxin than that expressed by transgenic plants. This work investigated the development and reproduction of T. urticae and of the predator Phytoseiulus macropilis Banks, during three successive generations looking for potential nontarget effect. In addition, behavioral studies on feeding preference, oviposition, and predation were carried out on Bt and non-Bt cottons. The development and reproduction of T. urticae and P. macropilis was conducted using leaf discs of Bt and non-Bt cottons. Arena containing leaf discs from both cotton types connected by a slide coverslip were also used in the behavioral studies. Averages of the three generations showed that the Bt-cotton does not affect the development, survival of immature stages, and reproductive output of T. urticae and of the predator P. macropilis. Furthermore, the preference for feeding and oviposition of T. urticae and P. macropilis were similar on both cotton types. In addition, P. macropilis exhibited similar predatory behavior on T. urticae fed on both cotton types. Levels of Cry1Ac toxin in T. urticae was 3.97 times greater than that found in the Bt-cotton plants as determined using a ELISA test. Despite of the amount of toxin acquired by the prey (T. urticae), no detectable levels of Cry1Ac were found in the predatory mite P. macropilis.